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BACKGROUND: To gain insight into the role of satellite cells in skeletal muscle hypertrophy, the effect of radiation on small fiber formation, embryonic myosin heavy chain (embryonic MHC) production, and insulin-like growth factor I (IGF-I) production in overloaded adult rat soleus muscle was examined. METHODS: Adult rat soleus muscle was overloaded by ablation of the synergistic gastrocnemius, plantaris, and flexor digitorum profundus muscles of the right hindlimb. Half of the rats were subjected to gamma irradiation of the right hindlimb prior to ablation in an attempt to prevent satellite cell proliferation. RESULTS: Wet weight of the non-irradiated overloaded soleus muscle increased almost 40% compared to contralateral control muscle following 4 weeks of overload. Small fibers, which were rare in control muscle, accounted for 6.76 +/- 5.08% to 12.74 +/- 7.76% of the total fiber number of the non-irradiated soleus following 1 to 4 weeks of overload. Although usually absent in control muscle, IGF-I or embryonic MHC was immunolocalized in a small percentage (< 11%) of the mature fibers in the non-irradiated overloaded soleus. Irradiation prevented compensatory hypertrophy and nearly abolished small fiber formation in the overloaded soleus. However, irradiation did not diminish the percentage of mature fibers producing immunocytochemically detectable levels of embryonic MHC or IGF-I. CONCLUSIONS: Irradiation may prevent hypertrophy by impairing activation, proliferation, and/or differentiation of satellite cells. Small fibers in overloaded muscle appear to be new fibers arising from satellite cells. IGF-I may have a role in muscle hypertrophy involving satellite cell activation, or perhaps a more direct role that requires additional factors.

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This study examined the role of longitudinal fiber splitting in enlarged anterior latissimus dorsi (ALD) muscle of adult quail. Muscle hypertrophy was induced using a model of progressive stretch overload (PSO) (5). After 16 and 28 d of PSO, muscle mass in the stretched ALD muscle increased significantly (P < 0.05) 188% and 294%, respectively, when compared with the intra-animal control muscle. Muscle length increased significantly (P < 0.05) in the stretched ALD muscle vs the intra-animal control by approximately 77% for both groups. Fiber number, which was assessed using direct counts after nitric acid digestion, did not change in the 16-d group; however, the 28-d stretched ALD muscle exhibited a 30% increase (P < 0.05) in fiber number vs the intra-animal control muscle. Furthermore, the frequency of splitting (i.e., branching) fibers was less than 0.3% in all muscles examined except the 28-d stretched ALD muscle. The 28-d stretched ALD muscle had 5.25% of its muscle fibers exhibiting split profiles. These results demonstrate that PSO produces effects unlike chronic stretch overload in that longitudinal fiber splitting may contribute significantly to an increase in fiber number.

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Skeletal muscle enlargement in adult animals has been ascribed primarily to changes in fiber cross-sectional area (i.e., fiber hypertrophy); however, recent evidence from several laboratories suggests strongly that fiber hyperplasia contributes to muscle mass increases in adult animals and possibly human athletes. Scientists have used three models to study the cellular mechanisms of muscle enlargement: compensatory hypertrophy, stretch, and exercise. Each of these models has provided direct as well as indirect evidence supporting the occurrence of muscle fiber hyperplasia. Direct counts of muscle fibers using nitric acid digestion techniques have shown that both exercise and stretch overload result in significant increases (range = 9-52%) in fiber number. Indirect fiber counts using histological cross-sections have suggested fiber hyperplasia (range = 10-82%) in all three models. Additionally, the expression of embryonic myosin isoforms have provided indirect evidence for new fiber formation in stretch overloaded muscle. Furthermore, satellite cells have been shown to be involved in muscle fiber hyperplasia in stretch and exercise.

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Intermittent stretch of the anterior latissimus dorsi (ALD) muscle produces fiber hypertrophy without fiber hyperplasia (J. Appl. Physiol. 74: 1893-1898, 1993). This study was undertaken to determine if a progressive increase in load and duration of stretch would induce extremely large muscle fiber areas or if the fibers would reach a critical size before the onset of fiber hyperplasia. Weights ranging from 10 to 35% of the bird's mass were attached to the right wing of 26 adult quail while the left wing served as the intra-animal control. The stretch protocol was as follows: day 1 (10% wt), days 2 and 3 (rest), day 4 (15% wt), days 5-7 (rest), day 8 (20% wt), days 9 and 10 (rest), days 11-14 (25% wt), days 15 and 16 (rest), and days 17-38 (35% wt). Birds were killed after 12, 16, 20, 24, and 28 days of stretch not including rest days. Muscle mass increased 174% (12 days), 196% (16 days), 225% (20 days), 264% (24 days), and 318% (28 days). Muscle length increased 60% (12 days), 34% (16 days), 59% (20 days), 50% (24 days), and 51% (28 days). Mean fiber area increased 111% (12 days), 142% (16 days), 75% (20 days), 90% (24 days), and 39% (28 days). Fiber number, which was measured histologically, increased significantly by 82% only in the 28 days of stretch group. The percentage of slow tonic fibers did not change for any of the time points examined.(ABSTRACT TRUNCATED AT 250 WORDS)

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In the chronic stretch model, muscle fiber hyperplasia precedes fiber hypertrophy [Alway et al. Am. J. Physiol. 259 (Cell Physiol. 28): C92-C102, 1990]. This study was undertaken to determine if an intermittent stretch protocol would induce fiber hypertrophy without fiber hyperplasia. A weight equalt to 10% of the bird's mass was attached to the right wing of seven adult quail while the left wing served as the intra-animal control. The weight was attached to the wing for 24-h periods interspersed with a 48- to 72-hr rest interval. The actual stretch time was 5 days while the length of the treatment period was 15 days. Muscle mass and length increased significantly 53.1 +/- 9.0 and 26.1 +/- 7.3% in the stretched anterior latissimus dorsi. Fiber number, which was determined from a histological section in the midregion of the muscle, did not change (control 1,651.6 +/- 94.8; stretch 1,626.0 +/- 70.9). The slow tonic fiber areas increased significantly an average of 28.6 +/- 5.7%, whereas the fast fibers increased 18.5 +/- 8.4% when compared with control values. Mean fiber area (average of slow and fast fibers) increased significantly by 27.8 +/- 6.0% in the stretched anterior latissimus dorsi. There were no differences in the percentage of slow fibers or volume density of noncontractile tissue. These data indicate that muscle adapts differently to intermittent stretch than it does to chronic stretch despite an equivalent load and stretch duration. In contrast to chronic stretch, 5 days of intermittent stretch produces muscle fiber hypertrophy without fiber hyperplasia.

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The structural and functional characteristics of the elbow flexors in five elderly males were studied before and after 12 wk of heavy-resistance training. Muscle volume and cross-sectional area of two of the elbow flexor (biceps brachii and brachialis) muscles were determined by magnetic resonance imaging. Mean muscle fiber area, percent fiber distribution, and collagen and noncontractile tissue densities were determined on histological sections from needle biopsies. Isokinetic strength of the elbow flexors was measured at velocities between 60 and 300 degrees/s. Muscle volume and cross-sectional area of the biceps brachii and brachialis significantly increased by 13.9 and 22.6%, respectively, after the training program. A preferential hypertrophy of type II fibers (37.2%) was observed. Significant increases in peak torque were observed at all the tested velocities. The amount of work a subject could perform during a 25-repetition test at 240 degrees/s increased by 41% after training. These results demonstrate that the skeletal muscles of elderly individuals can adapt to heavy-resistance exercise and do so by increases in both muscle size and strength.

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To determine if there is a correlation between the degree of delayed increase in signal intensity (SI) of muscle after exercise on magnetic resonance (MR) images and the amount of ultrastructural (ULS) injury and delayed-onset muscle soreness (DOMS), MR imaging-guided muscle biopsy was performed to obtain tissue from the legs of nine sedentary subjects 48 hours after downhill running on a treadmill. The degree of soreness was subjectively graded. T1-weighted, spin-density, T2-weighted, and short inversion time inversion-recovery images were obtained before and after biopsy, at 48 and 96 hours after exercise, respectively. The delayed SI increase of muscle on images obtained before biopsy was subjectively graded and measured. The degree of ULS injury was determined with electron micrographs. Serum creatine kinase levels were obtained before and up to 144 hours after exercise at 24-hour intervals. The measured SI, SI grades, and DOMS grades were correlated with the degree of ULS injury. Linear regression analysis revealed poor correlation between the DOMS grades and the degree of ULS injury and good correlation between the SI grade and the degree of ULS injury.

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We have measured capillary distribution in costal and crural canine diaphragm using two methods: histochemical processing and perfusion fixation. Each of 18 dogs was deeply anesthetized, the abdomen opened, and the left inferior phrenic artery cannulated. The animal was heparinized and overdosed with pentobarbital. The right hemidiaphragm was frozen, either postexcision (Protocol 1) or intact with no preload (Protocol 2), for histochemical processing. The left hemidiaphragm was fixed by perfusion in situ using 2% glutaraldehyde, either with preload (Protocol 1) or without (Protocol 2). Costal and crural regions of each hemidiaphragm were sampled for analysis. Frozen samples were sectioned and processed for acid-stable (pH 4.0) ATPase activity; perfusion-fixed samples were postfixed, stained, embedded in Epon, and sectioned. Measurements were made using a digital imaging system. We found that muscle fibers had smaller cross-sectional areas in costal than in crural diaphragm; capillary-to-fiber ratio (C:F) did not differ by region and regional differences in capillary density could be attributed to differences in fiber size. Results depended critically on methodology. In perfusion-fixed muscle, fiber area was less, C:F was greater, and capillary density was greater than in histochemically-processed tissue. We conclude that capillary distribution is similar in costal vs. crural diaphragm and that perfusion fixation identifies capillaries more effectively than histochemistry.

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Although exercise-induced muscle fiber hyperplasia has been demonstrated through direct fiber counts following nitric-acid digestion of muscle, morphological studies to determine the mechanism of hyperplasia have not been performed previously. In this study, light and electron microscopy were used to evaluate evidence of muscle fiber splitting or de novo formation of new muscle fibers. Since both fiber hypertrophy and hyperplasia may result in alterations in the muscle nuclear populations, myonuclear number and satellite cell frequency were assessed quantitatively to determine their role in regulating muscle fiber size. Ten adult cats performed weight-lifting exercise, and the right (exercised) and left (control) forelimbs were fixed by vascular perfusion. Spaced serial sections were used to evaluate muscle fiber morphology along the length of fibers, and muscle fiber areas were measured. Myonuclei and satellite cells were counted using electron microscopy. Morphological evidence supporting muscle fiber hyperplasia was observed in exercised muscles. These observations included the presence of small fibers which may signify de novo fiber formation. Myonuclear counts indicate that myonuclear density is not a primary regulator of fiber size. Satellite cell frequency was unchanged following exercise. Autoradiographic studies revealed satellite cell activation by uptake of tritiated thymidine in exercised muscles. Satellite cell activation appears to result from increased activity in exercised muscles. These findings confirm previous studies demonstrating muscle fiber hyperplasia following weight-lifting exercise, and suggest that de novo fiber formation is the major mechanism contributing to muscle fiber hyperplasia in this model.

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In the avian stretch model, the application of a weight overload to the humerus induces enlargement of the anterior latissimus dorsi (ALD) muscle and an increase in muscle fiber number which is accompanied by satellite cell activation. Myofiber injury may be an important stimulus to muscle fiber hyperplasia; therefore, light and electron microscopic evaluation was undertaken to determine if myofiber injury occurs in the stretch-enlarged ALD muscle of the adult quail. Autoradiographic studies were used to determine the terminal differentiation of labeled myogenic cells. A weight equal to 10% of body mass was attached to one wing of 27 adult quail and 3 birds were euthanized at 9 intervals of stretch, from 1 to 30 days. Birds were injected with tritiated thymidine at intervals ranging from 1 hr to 3 days prior to euthanization. Labeled nuclei were detected by light microscopic examination and identified by electron microscopy of a serial section. Three regions of the muscle were examined for disorganization of contractile elements, presence of cytoplasmic vacuoles, and/or phagocytic cell infiltration. The percentage of fibers exhibiting one or more of these criterion was significantly greater in the stretched ALD by Days 5 and 7 and declined at Day 10, reaching near control values by Day 14. Myofiber necrosis and phagocytic cell infiltration were only observed in the middle and distal regions of the stretched ALD muscle. Traditional signs of regeneration and repair were observed, including clusters of labeled myoblast-like cells and myotube formation within an existing basal lamina. New myotube formation with labeled central nuclei was also noted in the interstitial space, outside of basal lamina of persisting fibers. Labeled myonuclei were observed in the stretched fibers. These results demonstrate that chronic stretch produces regional injury and fiber degeneration and resultant regeneration in the ALD muscle of the adult quail. This may be an important stimulus for new fiber formation in this model.

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The influence of gender on muscular adaptation of the elbow flexors to 24 wk of heavy resistance training was studied in five male bodybuilders (MB) and five female bodybuilders (FB) who were highly competitive. Muscle cross-sectional area (CSA), fiber area, and fiber number were determined from the biceps brachii, and voluntary elbow flexor torque was obtained at velocities of contraction between 0 and 300 degrees/s. Biceps and flexor CSA was 75.8 and 81% greater, respectively, in MB than in FB, but muscle CSA was not significantly altered by the training program in either group. Because estimated fiber number and the volume density of nonmuscle tissue were similar in MB and FB, most of the gender difference in muscle CSA appeared to be due to greater absolute mean fiber areas in MB (10.51 and 10.68 x 10(3) microns 2 pre- and posttraining, respectively) than in FB (5.33 and 5.96 x 10(3) microns 2 pre- and posttraining, respectively). In neither MB nor FB did fiber type achieve further hypertrophy during the 24-wk training program. These data suggest that the extent of any change in muscle mass or muscle fiber characteristics is minimal after a bodybuilder of either gender has attained a high degree of muscle mass and a highly competitive status.

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Satellite cell frequency was assessed in control and stretched anterior latissimus dorsi (ALD) muscles of adult quail. A weight equal to 10% of body mass was attached to one wing for time intervals ranging from 1-30 days. The contralateral ALD served as the intra-animal control. Satellite cell frequency, expressed as a percentage of total myofiber nuclei within the basal lamina, was determined in eight control and stretched ALD muscles, that had been weighted for 5, 7, or 10 days. Satellite cell frequency was determined in 584 control and 473 stretched fibers and was not different in the control or stretched ALD muscles (15.6 +/- 2.3%, 16.7 +/- 6.1%, respectively). The number of myofiber nuclei (myonuclei and satellite cell nuclei) was examined in whole fiber segments from control and stretched ALD muscles of 27 adult quail. Nuclear frequency was determined in 500 control and 1,200 stretched fiber segments. Fiber volume was calculated from fiber length and diameter measurements. Nuclear number normalized to 10,000 microns 3 fiber volume was correlated to fiber cross-sectional area (P less than 0.0001). Fibers with cross-sectional areas less than 500 microns 2 had a greater nuclear to fiber volume ratio compared to fibers with areas greater than 500 microns 2. The nuclear-to-cytoplasmic ratio was not constant in smaller fibers. Nuclear density decreased as fiber cross-sectional area increased up to 500 microns 2. Fibers with cross-sectional areas greater than 500 microns 2 demonstrated a constant nuclear-to-cytoplasmic ratio. The results demonstrate that absolute nuclear number increased to maintain a constant nuclear-to-cytoplasmic ratio in the stretched hypertrophied fibers. Daughter cells originating from activated satellite cells may have contributed to the myonuclear population to maintain a constant nuclear-to-cytoplasmic ratio in the hypertrophied fibers of the adult quail.

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Progressive resistance exercise was used to induce hypertrophy in the right palmaris longus muscle (PLM) of 16 cats. The left PLM served as the non-exercised intra-animal control. After an average 150 +/- 26.6 wk of training, left and right PLMs were removed and weighed. Muscle fibers were typed using standard histochemical techniques. Mean fiber cross-sectional area, connective tissue content, and muscle fiber length were determined. The right exercised PLM demonstrated a 24.2 +/- 6.9% increase in muscle mass. Mean muscle fiber cross-sectional area increased 11.0 +/- 7.3% in the exercised muscles. No change in connective tissue content, fiber length, or fiber type composition was observed. The results show that increases in muscle fiber cross-sectional area do not account for all the observed increases in muscle mass, and that other mechanisms, such as muscle fiber hyperplasia, may play a role in contributing to muscle mass increases.

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Satellite cell activity was examined in the stretch-enlarge anterior latissimus dorsi muscle (ALD) of the adult quail. Thirty-seven birds had a weight equal to 10% of their body mass attached to one wing while the contralateral wing served as an intra-animal control. At various time intervals after application of the wing weight (from 1 to 30 days), the birds were injected with tritiated thymidine and killed 1 h later. Stretched muscle length was greater by day 1 and mass by day 3 when compared with the contralateral muscle. Satellite cells actively synthesizing DNA were quantitated in fiber segments of the control and stretched ALD. A minimum of 1,500 muscle nuclei (satellite cell nuclei and myonuclei) were counted in each muscle. Labeling in stretched muscle was expressed by the percent labeled nuclei per total nuclei counted. Satellite cell labeling was initiated by day 1, peaked between days 3 and 7, and was not statistically different from control values at day 30. These results demonstrate that satellite cells are induced to enter the cell cycle in the stretch-enlarged ALD muscle from the adult quail, and the peak of proliferative activity is within the first week of stretch.

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When skeletal muscle is subjected to stretch it undergoes a rapid increase in muscle mass. However, the effect of stretch on the native myosin isozyme content of muscle has received attention only recently. Using the Japanese quail to investigate stretch-induced hypertrophy, we demonstrated an increase in the expression of fast myosin in the predominantly slow anterior latissimus dorsi muscle (ALD). The fast myosin content of the control quail ALD is not sufficient to be quantified on native myosin pyrophosphate gels. After 33 days of stretch, the fast myosin content (N = 10) averaged 16 +/- 11% in the stretched muscles and reached a maximum of 40%. Mean hypertrophy in the stretched muscle, as indicated by muscle weight, was 247 +/- 91% (range, 168-378%). Fast myosin was consistently expressed in muscles with hypertrophy greater than 250%. Muscle fiber size from the stretched muscles contained a greater number of fibers with small cross-sectional areas than was observed in controls. These results indicate that substantial remodeling occurs in the stretched ALD muscle of the Japanese quail.

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The contributions of fiber hypertrophy and new fiber formation to the onset of stretch-induced muscle enlargement were evaluated in the anterior latissimus dorsi (ALD) of adult Japanese quails, because it was not known whether the mechanisms which initiate new fiber formation were dependent on first achieving significant fiber hypertrophy. A weight corresponding to 10% of the bird's body mass was attached to one wing, and eight birds were killed after each day during the first week of stretch. Muscle mass was significantly increased after 48 h of stretch; however, the elevation in nonmuscle tissue accounted for this increase. Muscle mass corrected for non-muscle tissue was significantly greater than the intra-animal control by the fourth day of stretch. Mean fiber cross-sectional area did not change during days 0-6, but cross-sectional area was 30.0 +/- 17.2% greater than the intra-animal control areas at day 7. Fiber number determined after nitric acid digestion of connective tissue was 27.1 +/- 5.8% greater than the intra-animal control at days 5-7 of stretch, but the number of fibers in the control muscles at days 5 and 6 were lower than at day 0. Thus new fiber formation was not preceded by significant fiber hypertrophy. These results fail to support a mechanism for new fiber formation which involves fiber splitting from hypertrophied myofibers during the first week of stretch.

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Eight elite male bodybuilders (MB), five elite female bodybuilders (FB), eight male control (MC), and eight female control recreational weight-trainers (FC) performed maximal elbow flexions on an isokinetic dynamometer at velocities between 1.02 and 5.24 rad.s-1, from which peak torque (PT) was measured. Elbow flexor cross-sectional area (CSA) was measured by computed tomographic scanning. Flexor CSA.lean body mass-1 ratios were greater in MB than in other subject groups. Correlations of PT were positively related to CSA but negatively to CSA.lean body mass-1 and to PT.CSA-1. PT.CSA-1 at low-velocity contractions were greater in MC and FC than in MB and FB groups, suggesting a training effect. The velocity-associated declines in torque between velocities of 1.02 and 5.24 rad.s-1 averaged 28.4 +/- 0.9% and were statistically identical in men and women among the subject groups, suggesting that neither gender nor training had affected this variable.

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This study was designed to examine the adaptive response of the human masseter muscle following surgical correction of abnormal facial form. Biopsies of the deep surface of the anterior superficial masseter muscle were obtained from five patients demonstrating vertical maxillary excess (VME), one at the time of corrective surgery, and a second at a long-term postoperative time interval (mean, 8 months). Control biopsies were also obtained from five individuals (three cadavers and two patients) with normal dentofacial morphology. A standard regimen of histologic and histochemical staining was used to classify individual muscle fibers as either type 1, type 2, or intermediate. In both VME patients and normal subjects type 1 fibers predominated, with the control group displaying a higher percentage (50% vs. 43%). On the average, type 1 fibers also had the largest areas. Following surgery there was an increase in type 2 fibers (30% vs. 52%). Two patients receiving maxillary surgery only exhibited either no change in mean fiber area or only a slight increase. The three remaining patients who underwent concomitant maxillary and mandibular surgery all showed a significant decrease in mean fiber area. Two persons in the latter group also showed features consistent with a denervation-reinnervation process. The results of this study indicate that the human masseter responds to surgical manipulation of the jaws in a histochemically demonstrable manner, with the nature and magnitude of the response associated with the particular surgical procedure(s) performed.

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Muscle cross-sectional area (CSA), fiber area, and fiber number were determined from the biceps brachii of eight elite male bodybuilders (MB) and five elite female bodybuilders (FB) who had similar training characteristics. Biceps CSA was obtained from computer tomographic scanning and corrected for noncontractile tissue. Biceps CSA was twofold greater in MB relative to FB and strongly correlated to lean body mass (R = 0.93). Biceps CSA expressed per kilogram lean body mass (LBM) or per centimeter body height (BH) was 35% greater in MB compared with FB. Most of the gender difference in muscle CSA was because of greater absolute mean fiber areas in MB (9,607 microns2) relative to FB (5,386 microns2); however, MB also had a significantly greater population of small type II fibers (less than 2,000 microns2) compared with FB. Type II fiber area/LBM averaged 1.6-fold greater in MB compared with FB; however, type I fiber area/LBM was similar between groups. Biceps CSA was positively correlated to fiber CSA (R = 0.75) and fiber number (R = 0.55). This suggests that adaptations to resistance training may be complex and involve fiber hypertrophy and fiber number (e.g., proliferation). Alternatively, since the muscle characteristics before training are not known, these apparent adaptations might be genetically determined attributes.

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